ACCEPTED. Rates and reasons of failure of commercial HIV-1 viral load assays in Brazil
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1 JCM Accepts, published online ahead of print on 28 March 2007 J. Clin. Microbiol. doi: /jcm Copyright 2007, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved. 1 Rates and reasons of failure of commercial HIV-1 viral load assays in Brazil Jan Felix Drexler 1,2, Luciano Luna de Souza 1, Celia Pedroso 2, Diana Brasil Pedral-Sampaio 2, Artur T.L. Queiroz 3, Carlos Brites 2, Eduardo M. Netto 2, Christian Drosten 1* 1 Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany 2 Laboratório de Pesquisa em Infectologia, Hospital Universitário Prof. Edgard Santos, Salvador, Brazil 3 Laboratório de Saúde Avançada, Fiocruz, Salvador, Brazil Address for correspondence Dr. Christian Drosten Bernhard Nocht Institute for Tropical Medicine Clinical Virology Section Bernhard Nocht Str Hamburg Germany Tel Fax drosten@bni-hamburg.de Running title: Viral load-assay failure in Brazil 957 words
2 2 Abstract We examined failures of commercial HIV-1 viral load assays in 1195 plasma samples from Brazilian patients. Assay failure was assumed in samples undetectable by commercial assay but positive by real-time RT-PCR for HIV-1 LTR region, or, if viral load differed by >2 Log10 against LTR assay. Failure rates for Bayer Versant 3.0, Roche Monitor V1.5, and Biomerieux NucliSens QT were 0.68%, 0.47%, 4.33% respectively. NucliSens may be inadequate for Brazil.
3 3 Worldwide over 38 million people are estimated to be infected with HIV-1 (15). About 630,000 of these live in Brazil. In Brazil, HIV infected individuals receive treatment free of charge, which creates one of the largest populations on antiretroviral therapy worldwide (1). The determination of viral load is an integral part of therapy, necessary to recognize treatment failure and to prevent transmission of resistant strains. However, commercial viral load assays were originally designed to detect subtype B viruses which are most prevalent in North America and Western Europe (14). It is likely that such assays will be less appropriate for other virus populations, and several earlier studies focused on this problem. Unfortunately, most studies used small numbers of clinical samples, in the range of 100 specimens (2, 5, 12, 13). No study has prospectively evaluated a routine testing program including all major viral load assays, and none used a uniform gold standard method for comparison. In view of the large numbers of patients under monitored therapy in Brazil, the significance of wrong viral load quantification was determined in this specific setting. We analyzed 1195 samples from three different regions of Brazil. In a recent multi-center study on HIV-1 quantification (7), viral loads had been tested in these samples with either Bayer Versant bdna 3.0, Merieux NucliSens HIV-1 QT or Roche Amplicor Monitor 1.5 assays. Viral loads were also determined in all samples with a new real-time RT-PCR test for the highly conserved 5 long terminal repeat (LTR) region. This assay detected non-b subtypes with improved efficiency (7). It served as our gold standard. We selected all samples testing negative in any of the three commercial assays, and showing viral loads above copies/ml at the same time by real time LTR RT-PCR. In addition, samples that were under-quantified by at least a factor of 100 in the commercial assays, as opposed to LTR PCR, were also included.
4 4 To make sure that underlying data were correct, all original LTR viral loads from the previous study were confirmed by re-testing with the LTR assay from original plasma. Viral loads from commercial assays were not re-tested since these were issued during ongoing treatment by certified Brazilian viral load laboratories, which are subject to strict quality control by the Brazilian Ministry of Health. As shown in Table 1, Bayer Versant bdna 3.0 and Roche Monitor 1.5 showed significant discrepancies in 0.68% and 0.47% samples, respectively. The NucliSens assay, however, gave discrepant results in 4.33% of tested samples. This rate was significantly higher than with the other commercial methods (χ 2 =20.36, p<0.0001). To exclude a systematic technical error in the gold standard method, 10 of the 14 samples discrepant by NucliSens were retested with Roche Amplicor (no material was left from the remaining four samples). Indeed, virus was detected by Amplicor in seven out of ten samples. The median discrepancy between LTR and Amplicor results was 0.95 Log 10 in the detected samples. For comparison, the median difference between LTR and NucliSens had been 4.44 Log 10. Reasons for failure were determined by sequencing of the gag and pol genes directly from samples. Phylogenetic analysis was performed using TreeCon 1.3. Phylogenetic typing was confirmed with Simplot (9), using the subtype reference alignment of the Los Alamos HIV database supplemented by extra Brazilian B, C, and F-subtype sequences (three per subtype). The numbers of mismatches for both the Monitor V1.5 and the NucliSens assays were highest in F, BF, C and CF samples (Figure 1). Both samples not detected by Monitor 1.5 had subtype F signatures in their amplicon target region (gag) and revealed a common mismatch pattern in the hybridization domain of the reverse primer. To our surprise the majority of discrepant samples for NucliSens contained pure subtype B viruses (11 of 14, Table 1); the others were also F- recombinants. Oligonucleotide mismatches are shown in Figure 1 for all BF recombinants and
5 5 four subtype B samples. For the remaining subtype B samples such mismatches could not be confirmed. Interestingly there are other recent reports on such observations, suggesting that oligonucleotide mismatches may not be the only reason for assay failure with the NuciSens system (2, 12). For the bdna assay it was not possible to determine the contribution of virus variability to misquantification because its 98 probes in the pol gene are unpublished. Its design should be relatively stable against nucleotide mismatches (8, 13). Interestingly, for two of the three samples misquantified with this assay the alignment in Figure 1 suggests that they would predictably fail with NucliSens and Monitor assays (no re-testing was possible due to lack of plasma). These viruses were C-subtypes or C-recombinants. This is the first study to permit a quantitative estimation of HIV-1 viral load assay failure within Brazil, one of the largest HIV-1 treatment settings worldwide. Approximately 83% of Brazilian HIV-1 strains are subtype B, 14% F and 3% C. Subtype C is predominant at up to 50% in the south of Brazil, whereas subtype F and B/F-recombinants predominate in the north at up to 50% (3, 4, 11, 17). The conformity of our samples with this spectrum of HIV-1 subtypes and the large number of samples analyzed justify extrapolation of our study to the Brazilian HIV-1 population. Currently, NucliSens is being applied in 32 of 73 Brazilian MOH reference laboratories for HIV-1 viral load determination, many of which are situated in regions with the highest prevalence of subtype F and F-recombinant viruses. 180,000 individuals are on antiretroviral therapy in Brazil, receiving up to four viral load determinations per year. Assuming these numbers, the observed rate of 4.3% samples undetectable or seriously underquantified with the Biomerieux NucliSens assay can be extrapolated to at least patients annually. It should be re-examined whether this assay is appropriate for Brazil at all.
6 6 Acknowledgements All nucleotide sequences determined in this study are available from GenBank, accession numbers EF EF The authors declare that they have no conflicts of interest. This study was partially funded by the Brazilian MOH grant CFA 273/04 and CFA 238/05. The Bernhard Nocht Institute receives funding from the German Ministry of Health for operating the National Reference Centre for Tropical Infectious Diseases. We are grateful to Daniel J. Morgan for revision of the manuscript, Carla Baroni from the Centro Biomédico da UFES - Núcleo de Doenças Infecciosas, Vitória/Espírito Santo and Mara Liane Rieck from Laboratório do Hospital Nossa Senhora da Conceição, Porto Alegre/Rio Grande do Sul for kindly contributing samples.
7 7 References 1. Anonymous A Experiência do Programa Brasileiro de Aids. Ministério da Saúde/Coordenação Nacional de DST e Aids. 2. Antunes, R., S. Figueiredo, I. Bartolo, M. Pinheiro, L. Rosado, I. Soares, H. Lourenco, and N. Taveira Evaluation of the clinical sensitivities of three viral load assays with plasma samples from a pediatric population predominantly infected with human immunodeficiency virus type 1 subtype G and BG recombinant forms. Journal of clinical microbiology 41: Bongertz, V., D. C. Bou-Habib, L. F. Brigido, M. Caseiro, P. J. Chequer, J. C. Couto-Fernandez, P. C. Ferreira, B. Galvao-Castro, D. Greco, M. L. Guimaraes, M. I. Linhares de Carvalho, M. G. Morgado, C. A. Oliveira, S. Osmanov, C. A. Ramos, M. Rossini, E. Sabino, A. Tanuri, and M. Ueda HIV-1 diversity in Brazil: genetic, biologic, and immunologic characterization of HIV-1 strains in three potential HIV vaccine evaluation sites. Brazilian Network for HIV Isolation and Characterization. J Acquir Immune Defic Syndr 23: Brindeiro, R. M., R. S. Diaz, E. C. Sabino, M. G. Morgado, I. L. Pires, L. Brigido, M. C. Dantas, D. Barreira, P. R. Teixeira, and A. Tanuri Brazilian Network for HIV Drug Resistance Surveillance (HIV-BResNet): a survey of chronically infected individuals. AIDS (London, England) 17: Burgisser, P., P. Vernazza, M. Flepp, J. Boni, Z. Tomasik, U. Hummel, G. Pantaleo, and J. Schupbach Performance of five different assays for the quantification of viral load in persons infected with various subtypes of HIV-1. Swiss HIV Cohort Study. Journal of acquired immune deficiency syndromes (1999) 23:
8 8 6. Christopherson, C., J. Sninsky, and S. Kwok The effects of internal primertemplate mismatches on RT-PCR: HIV-1 model studies. Nucleic acids research 25: Drosten, C., M. Panning, J. F. Drexler, F. Hansel, C. Pedroso, J. Yeats, L. K. de Souza Luna, M. Samuel, B. Liedigk, U. Lippert, M. Sturmer, H. W. Doerr, C. Brites, and W. Preiser Ultrasensitive monitoring of HIV-1 viral load by a lowcost real-time reverse transcription-pcr assay with internal control for the 5' long terminal repeat domain. Clinical chemistry 52: Jagodzinski, L. L., D. L. Wiggins, J. L. McManis, S. Emery, J. Overbaugh, M. Robb, S. Bodrug, and N. L. Michael Use of calibrated viral load standards for group M subtypes of human immunodeficiency virus type 1 to assess the performance of viral RNA quantitation tests. Journal of clinical microbiology 38: Lole, K. S., R. C. Bollinger, R. S. Paranjape, D. Gadkari, S. S. Kulkarni, N. G. Novak, R. Ingersoll, H. W. Sheppard, and S. C. Ray Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. Journal of virology 73: Michael, N. L., S. A. Herman, S. Kwok, K. Dreyer, J. Wang, C. Christopherson, J. P. Spadoro, K. K. Young, V. Polonis, F. E. McCutchan, J. Carr, J. R. Mascola, L. L. Jagodzinski, and M. L. Robb Development of calibrated viral load standards for group M subtypes of human immunodeficiency virus type 1 and performance of an improved AMPLICOR HIV-1 MONITOR test with isolates of diverse subtypes. Journal of clinical microbiology 37: Soares, M. A., T. De Oliveira, R. M. Brindeiro, R. S. Diaz, E. C. Sabino, L. Brigido, I. L. Pires, M. G. Morgado, M. C. Dantas, D. Barreira, P. R. Teixeira, S. Cassol,
9 9 and A. Tanuri A specific subtype C of human immunodeficiency virus type 1 circulates in Brazil. Aids 17: Swanson, P., C. de Mendoza, Y. Joshi, A. Golden, R. L. Hodinka, V. Soriano, S. G. Devare, and J. Hackett, Jr Impact of human immunodeficiency virus type 1 (HIV-1) genetic diversity on performance of four commercial viral load assays: LCx HIV RNA Quantitative, AMPLICOR HIV-1 MONITOR v1.5, VERSANT HIV-1 RNA 3.0, and NucliSens HIV-1 QT. Journal of clinical microbiology 43: Swanson, P., V. Soriano, S. G. Devare, and J. Hackett, Jr Comparative performance of three viral load assays on human immunodeficiency virus type 1 (HIV- 1) isolates representing group M (subtypes A to G) and group O: LCx HIV RNA quantitative, AMPLICOR HIV-1 MONITOR version 1.5, and Quantiplex HIV-1 RNA version 3.0. Journal of clinical microbiology 39: Takeb, E. Y., S. Kusagawa, and K. Motomura Molecular epidemiology of HIV: tracking AIDS pandemic. Pediatrics international 46: UNAIDS Report on the global AIDS epidemic. Joint United Nations Programme on HIV/AIDS/World Health Organization. 16. van Gemen, B., R. van Beuningen, A. Nabbe, D. van Strijp, S. Jurriaans, P. Lens, and T. Kievits A one-tube quantitative HIV-1 RNA NASBA nucleic acid amplification assay using electrochemiluminescent (ECL) labelled probes. Journal of virological methods 49: Vicente, A. C., K. Otsuki, N. B. Silva, M. C. Castilho, F. S. Barros, D. Pieniazek, D. Hu, M. A. Rayfield, G. Bretas, and A. Tanuri The HIV epidemic in the Amazon Basin is driven by prototypic and recombinant HIV-1 subtypes B and F. J Acquir Immune Defic Syndr 23:
10 von Truchsess, I., B. Harris, H. M. Schatzl, and J. Hackett, Jr The first B/G intersubtype recombinant form of human immunodeficiency virus type 1 (HIV-1) identified in Germany was undetected or underquantitated by some commercial viral load assays. Journal of medical virology 78:311-7.
11 11 Table 1 Undetectable or under-quantified samples Assay Roche Monitor V1.5 Bayer Versant V3.0 NucliSens HIV-1 QT (n deviant samples/sample s tested) Subtype a (p24/pol) Number of samples Log deviation c (2/430) (3/442) (14/323) F/F FB/BF B/B C/C F/C B/B F/rec b ( ) 3.99 ( ) a Phylogenetic analysis comprised HXB2 genome residues and HXB Primer sequences used for amplification and sequencing were: HXB , , , , , , (sense) and , , , , , , (antisense). Typing of circulating recombinant form was based on SimPlot analysis of gag (p24)/pol genes. b comprises one F/B, F/BF, F/FB gag (p24)/pol recombinant sample, respectively c Log10 (LTR assay - commercial assay), median (range)
12 12 Legend to Figure 1 Nucleotide mismatches at oligonucleotide binding sites of (A) Amplicor Monitor V1.5 and (B) NucliSens HIV-1 QT assay in the gag p24 gene. Samples HU-EFS and HI-LRM had been under-quantified by Monitor V1.5. Samples had been underquantified by NucliSens. Samples RS 310 RS 481 had been under-quantified by bdna V3.0. Primer and probe sequences were obtained from (10) and (6) for Monitor V1.5 and (16) and (18) for NucliSens, respectively.
13
Laboratory for Clinical and Biological Studies, University of Miami Miller School of Medicine, Miami, FL, USA.
000000 00000 0000 000 00 0 bdna () 00000 0000 000 00 0 Nuclisens () 000 00 0 000000 00000 0000 000 00 0 Amplicor () Comparison of Amplicor HIV- monitor Test, NucliSens HIV- QT and bdna Versant HIV RNA
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